Landscape and Cattle Management Attributes Associated with the Incidence of Desmodus Rotundus Attacks on Cattle

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Landscape and cattle management attributes associated with the incidence of Desmodus rotundus attacks on cattle

Article · January 2020 DOI: 10.19136/era.a6n18.2164

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Landscape and cattle management attributes associated with the incidence of Desmodus rotundus attacks on cattle

Características del paisaje y de manejo ganadero asociadas a la incidencia de ataques al ganado bovino por Desmodus rotundus

Karla Lanzagorta-Valencia1 , José Ignacio Fernández-Méndez2 , Rodrigo A. Medellín1 , Alba Z. Rodas-Martínez3 , Rafael Ávila-Flores1,3∗

1Instituto de Ecología, Universidad Nacional Autónoma de México, Circuito Exterior S/N Anexo Jardín Botánico Exterior, Ciudad Universitaria, 04510 Coyoacán, Ciudad de México, México. 2Instituto Nacional de Pesca, Av. México #190 Col. El Carmen, 03310 Coyoacán, Ciudad de México, México. 3División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, km 0.5 Carr. Villahermosa-Cárdenas S/N, entronque a Bosques de Saloya, 86039 Villahermosa, Tabasco, México. ∗Corresponding author: [email protected]

Scientiﬁc article received: February 28, 2019 accepted: August 06, 2019

ABSTRACT. Bovine paralytic rabies, transmitted by Desmodus RESUMEN. La rabia paralítica bovina, transmitida por Desmodus rotundus, causes economic losses for Latin American livestock rotundus, provoca pérdidas económicas al sector ganadero lati- producers. Although the total number of reported cases has noamericano. Aunque el número total de casos notificados ha decreased markedly due to vaccination campaigns, economic disminuido notablemente debido a las campañas de vacunación, losses can be significant for smallholders. Identifying risk fac- las pérdidas económicas pueden ser significativas para pe- tors for vampire bat attacks on cattle could help guide preven- queños propietarios. Identificar factores de riesgo podría ayudar tive control efforts in specific areas. The objective of this study a orientar esfuerzos de control preventivo en zonas específicas. was to analyze the relationship between the incidence of D. ro- El objetivo de este trabajo fue analizar la relación entre la inciden- tundus attacks on cattle and various landscape features and cia de mordeduras por D. rotundus y diversos atributos pisajís- cattle management practices in northeastern Puebla, Mexico. ticos y de manejo ganadero en el noreste de Puebla, México. We visited 61 properties with cattle between May and October Se visitaron 61 propiedades con ganado entre mayo y octubre 2011, in which we quantified the incidence of attacks on cattle de 2011; en cada sitio se cuantificó la incidencia de ataques al and described landscape and cattle management attributes. The ganado y se describieron las características del paisaje y del following features were described within a 200-m radius around manejo ganadero. En un radio de 200 m alrededor del sitio de the nightly resting site of cattle: topography, percent forest cover, descanso nocturno del ganado, se registró: topografía, cobertura and number of forest fragments, rivers and streams, tree lines, vegetal y número de fragmentos vegetales, ríos y arroyos, líneas buildings, roads and highways. With these variables, we built de árboles, construcciones humanas, carreteras y autopistas. models that were assumed to describe the levels of human in- Con estas variables, se construyeron modelos que describieron: terference, prey availability, and movement facilitation for bats. facilitación de movimiento, niveles de interferencia humana y The human interference model (number of buildings plus num- disponibilidad de presas para los murciélagos. El modelo de in- ber of roads) best explained the incidence of attacks on cattle. terferencia humana (número de construcciones más número de According to our results, the cattle with the highest vulnerability caminos) fue el que mejor explicó la incidencia de ataques. Los to attacks by vampire bats are those resting at night in less con- resultados sugieren que el ganado más vulnerable a los ataques fined sites, far away from human activity. Results of this study de vampiros es el que descansa por la noche en sitios menos suggest that rabies vaccination campaigns on cattle should focus confinados y lejos de la actividad humana. Se propone que las on fragmented areas with few livestock management practices. campañas de vacunación contra la rabia bovina se concentren Key words: Fragmentation, cattle ranching, vampire bat, Puebla, en áreas fragmentadas con escasas prácticas de manejo. rabies. Palabras clave: Fragmentación, ganadería, murciélago vampiro, Puebla, rabia.

DOI: 10.19136/era.a6n18.2164 www.ujat.mx/era ISSN: 2007-9028 E. ISSN: 2007-901X 1 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

INTRODUCTION Identifying risk zones is very useful in guiding preventive vaccination efforts in areas where livestock Bovine paralytic rabies represents one of the are most vulnerable to attacks by D. rotundus. The main problems for cattle ranching in the tropical re- few studies conducted on this subject suggest that the gions of the Americas (Lee et al. 2012). The disease, incidence of attacks on livestock seems to be related caused by a virus of the genus Lyssavirus (family to landscape attributes, especially those that describe Rhabdoviridae), has a long incubation period culmi- the distribution of forested areas. For example, in the nating in an acute and lethal course (Fisher et al. state of Sao Paulo, Brazil, riparian zones are reported 2018). Bovine paralytic rabies is usually transmitted to be landscape elements that facilitate attacks on by an infected animal biting a susceptible one, as livestock, because they favor the presence of suitable the virus is present in the saliva of sick animals. To roosts for D. rotundus (Taddei et al. 1991). However, date, the only known vector of this virus to livestock a study conducted in four municipalities in the same is the common vampire bat (Desmodus rotundus), Brazilian state found that rivers are not associated which feeds opportunistically on the blood of various with the risk of D. rotundus attacks on cattle (Gomes mammalian species (Johnson et al. 2014). et al. 2007). In another study conducted in the state of Cases of bovine rabies are geographically Sao Paulo, it was found that pastures with the highest limited to the distribution area of D. rotundus, which number of reported attacks on cattle tended to be ranges from Tamaulipas, Nuevo León, Sonora and surrounded by forest and sugarcane crops (Gomes Chihuahua in Mexico, to central Chile, northern Ar- et al. 2010). Recently, it was reported that some feral gentina and southern Brazil (Zarza et al. 2017). pigs were attacked by D. rotundus in an oil palm frag- In the last 50 years, the total number of reported ment surrounded by pastures, but not in other loca- cases in Latin America has decreased by several or- tions (Hernández-Pérez et al. 2019). In contrast, a ders of magnitude, largely as a result of intense pre- study conducted in the Bolivian Prepuna reported that ventive vaccination campaigns (Arellano-Sota 1988). the incidence of attacks on stabled goats was more However, bovine rabies continues to be a problem associated with the characteristics of the stockyards that generates significant economic losses for the than with the characteristics of the vegetation (Moya livestock sector. For example, between 1993 and et al. 2015). This suggests that livestock manage- 2002, 31 187 cases of bovine rabies were reported in ment strategies may affect the likelihood of a domestic Latin America (Belotto et al. 2005). In Mexico, in re- animal being attacked. For example, it has been recent years, rabies outbreaks have spread to regions ported that cows that disperse inside pastures during where they had previously not occurred (Bárcenas- the night are less attacked than those that are kept Reyes et al. 2015). It is difficult to establish the pre- together (Delpietro and Russo 1996), while stabled cise amount of losses caused by bovine rabies, as animals (pigs) tend to be more attacked than those cases usually occur in livestock areas where access (cows) that move freely near villages (Bobrowiec et to veterinary services is insufficient, there is little al. 2015). or no notification by producers, in many cases due This paper is founded on the assumption that to lack of knowledge of the disease or difficulty in the attributes analyzed (vegetation cover, topography, communicating with the corresponding authorities, river distribution, prey abundance, prey accessibility and diagnostic laboratories are limited (Acha and and distribution of anthropogenic activities) facilitate Málaga-Alba 1988). In this context, some authors or limit encounters between D. rotundus and its po- have proposed that for every reported case of rabies, tential prey at a specific point in the landscape. The there could be 10 that go unreported (Fornes et al. region studied, located within the distribution range 1974). Considering the underreporting, annual mor- of D. rotundus, is one of the most important livestock tality in the whole region could be close to 50 000 areas in the state. Therefore, the objective was to head of cattle (Acha and Szyfres 2003). analyze the relationship between various landscape

www.ujat.mx/era DOI: 10.19136/era.a6n18.2164 ISSN: 2007-9028 E. ISSN: 2007-901X 2 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

and livestock management attributes described in centrated during the night before the inspection (see situ with the incidence of cattle attacks by D. rotun- next section). The precise nightly resting site was dus in ranches in the northeast of the state of Puebla, identified with the help of farm staff. The sampling Mexico. The results of the study provide elements that unit’s perimeter was identified with the help of a GPS, can help delineate livestock management strategies and each unit had to be separated by at least 1 km that reduce the likelihood of the rabies virus being from the nearest unit to maximize data independence. transmitted to cattle. These types of preventive ac- The scale was selected to obtain a representative tions are crucial considering that population control of description of each property, assuming that each the vector has not proven to be an efficient measure sampling unit includes the most relevant landscape for bovine rabies control (Streicker et al. 2012). features that facilitate or limit access to prey for vampires. Each location was visited only once between MATERIALS AND METHODS the months of May and October 2011, allowing us to maximize the number of properties visited within Study area a short timeframe. In each sampling unit, the cattle The study was conducted in the northeast were inspected to estimate the incidence of attacks by of the state of Puebla, a region with a long cattle the vampire bat and data were collected on landscape ranching tradition and great potential for low-cost and livestock management attributes. meat and milk production within the state, due to the high availability of good-quality inputs and forage. The Cattle inspection study area is located within the Tuxpan-Nautla hydro- The cattle were checked only once in each logical region, which includes part of the Sierra Madre location to identify the individuals that had been Oriental and the Gulf Coastal Plain. In this region, attacked by D. rotundus. The inspection was carried the predominant climate is warm humid with year- out in the mornings to take advantage of each ranch’s round rainfall or abundant summer rainfall, and semi- own activities such as milking, vaccination and tick warm humid with year-round rainfall; the average dip. When possible, cows were placed in the handling annual temperature ranges from 22 to 30 ◦C. The chute with one person on each side to check both original vegetation includes portions of tropical ever- flanks for bites. The entire body was checked, paying green forest, pine-oak forest, cloud forest and cha- greater attention to the base of the ears, neck, udders, parral. Currently, agricultural zones are combined tail and legs, which are usually the parts of the body with fragments of natural vegetation dominated by most attacked by D. rotundus. For the purposes of subperennial tropical forest and cloud forest with this study, only recent bat bites were recorded, that varying degrees of disturbance (INEGI 2016). is, the cow had to be attacked the night before the day of the inspection. The criterion to identify recent Sampling design bites was to observe a line of fresh or semi-dry blood We selected a sample of 61 locations (villages, just below the wound, since the cow may have had ranches, rural settlements, hamlets and houses; bites prior to that night. At least 10 cows of any race, Figure 1) with the presence of livestock, mainly cattle, sex and age were reviewed, always by the same ob- that at the time of being visited had a minimum of server. Based on these data, the incidence of attacks 10 head. The locations were selected based on the per sampling unit was estimated and defined as the facilities granted by the owners, covering most of the percentage of individuals that were attacked at night highways and roads in the northeast of the state, relative to the total number of individuals checked. and trying to cover as much geographical area as possible. In each location, a 200-m radius circle (12.6 Description of sampling units ha) was established as the sampling unit, taking as The landscape and cattle management its center the area where the focal livestock was con- characteristics described for each sampling unit were

DOI: 10.19136/era.a6n18.2164 www.ujat.mx/era ISSN: 2007-9028 E. ISSN: 2007-901X 3 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

Figure 1. Distribution of 61 locations (sampling units) in the northeastern region of the state of Puebla, Mexico. selected considering ecological aspects of D. rotun- Data analysis dus, including attributes that might favor or limit its Simple correlation analyses were performed presence. The landscape attributes described in the to identify variables that might be related to field were (the categories are mentioned in paren- the incidence of attacks. Additionally, we per- theses in ascending order of valuation): dominant formed correlation analyses between all explanatory topography (flat, semi-undulating, undulating), num- variables to identify redundant variables (r ≥ 0.8), ber of rivers, number of streams, number of small eliminating those that showed the lowest correlation fragments of tree vegetation (each made up of 10 value with the response variable. Generalized linear trees and covering < 50% of the sampling unit), models (GLMs) with negative binomial error were number of large fragments of tree vegetation (each used to explore the relationship between the inci- covering ≥ 50% of the sampling unit), percent forest dence of attacks (%) and different combinations of cover, number of tree lines (live fences), number the explanatory variables. To do this, landscape and of roads and highways, and number of enclosed cattle management variables were grouped into three buildings (including houses, warehouses and sta- models based on ecological considerations: 1) move- bles). Livestock management attributes considered ment facilitation model: number of large vegetation were: type of location (ranch, house, village), type fragments, number of small vegetation fragments, of management (stabling, semi-stabling, controlled number of rivers and streams, number of tree lines, grazing, free grazing), type of confinement (village, type of topography and percent vegetation; 2) human stable, corral, pasture, large undelimited areas), num- interference model: number of buildings and number of head of cattle within a 200-m radius, size of ber of roads; and 3) prey availability model (which, herd examined and number of head of other livestock according to our hypothesis, is dependent on cattle species within a 500-m radius (in this case, the scale management): type of management, size of herd was extended to have a greater record of individuals). examined, number of head of cattle in 200 m and number of head of other livestock in 500 m. The

www.ujat.mx/era DOI: 10.19136/era.a6n18.2164 ISSN: 2007-9028 E. ISSN: 2007-901X 4 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

overall performance of each model was assessed of attacks on cattle. by the proportion of deviance that is explained by The inclusion of the most significant variables the variables considered (Pseudo-R2). The Akaike of each model improved the performance of the com- Information Criterion (AIC) was used to identify the bined model, although the deviance explained re- model that explains with the greatest parsimony the mained at very low levels (Table 1). In the combined differences in incidence of attacks between ranches. model, the number of individuals of other livestock species within a 500-m radius emerged as an impor- RESULTS tant variable (Table 2). According to the value of the β coefficient, it can be inferred that a greater local The average incidence of D. rotundus bites on abundance of production animals (other than cows) cattle was 7.8%. In other words, almost eight out of is related to a lower incidence of attacks on cattle every 100 cows in the northeastern region of the state (Figure 4). of Puebla were bitten every night by hematophagous bats between May and October 2011. However, the DISCUSSION spatial distribution of the bites was not homogeneous. While 26 properties (42.6% of the total) did not report In this study, some factors related to the inci- any bites during the evaluated period, three ranches dence of attacks on cattle by the common vampire recorded an incidence of bitten cows of between 30 bat (D. rotundus) were identified. Results suggest that and 40%. the attributes of the immediate landscape surrounding Univariate correlation analyses showed that, the sites where cattle rest at night (200 m around) taken independently, the evaluated variables were influence the probability of individuals being attacked little related to the incidence of attacks. Only the by D. rotundus. The trends detected, although sta- number of roads within a 200-m radius showed a sig- tistically insignificant, are compatible with existing nificant (negative) relationship with the incidence of knowledge of different ecological aspects of the attacks (r = -0.290, P = 0.024; Figure 2), suggesting common vampire bat. that the sites most traveled by vehicles and humans The model that included variables related to hu- were avoided by D. rotundus. man interference was the one that best explained the Pseudo-R2 values indicate that the constructed incidence of bat attacks on cattle in the northeastern models (GLMs) explained a low proportion of the to- region of Puebla. According to this model, D. ro- tal variation in the data (Table 1). Among them, tundus avoids attacking cows resting in sites with in- the model that best explained the incidence of cattle tense human activity, that is, sites surrounded by mul- attacks was that of human interference, which con- tiple roads and buildings. These results agree with sisted of the number of roads and the number of other studies where it has been found that individuals buildings. Within this model, the variable most re- of this species tend to move away from areas with lated to the incidence of attacks was the number of intense human activity. Although D. rotundus has roads within a 200-m radius (Table 2). The value of been recorded in large urban centers in Brazil, its the β coefficient suggests that the greater the number presence appears to be associated with large forested of roads around the cows’ resting site, the lower the or peripheral areas of cities (Dantas-Torres et al. incidence of attacks, and although its effect was sta- 2005, Esbérard et al. 2014), suggesting that evasion tistically less significant, the number of constructions of areas with intense human activity occurs at small also had a negative relationship with the incidence scales, such as those analyzed in this paper. of attacks (Figures 2 and 3). Although the relation- It is likely that the distancing of D. rotundus from ships were not significant, it can be observed that the areas with intense human activity is largely due to the sites with the greatest presence of anthropogenic ele- presence of artificial lighting, as would be expected in ments (roads and buildings) exhibited a low incidence species that naturally avoid high levels of luminosity.

DOI: 10.19136/era.a6n18.2164 www.ujat.mx/era ISSN: 2007-9028 E. ISSN: 2007-901X 5 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

Figure 2. Relationship between the incidence of attacks on cattle and the number of roads in 61 sampling units in northeastern Puebla. Pearson’s correlation coefﬁcient showed that this relationship was signiﬁcant (r = -0.290, P = 0.024).

Table 1. Statistical performance of three models that predict the incidence of cattle attacks by D. rotundus in 61 sampling units in the northeast of the state of Puebla. Residual deviance, Akaike Information Criterion (AIC) and Pseudo-R2 are reported. The variables considered were: number of large vegetation fragments (LVF), number of small vegetation fragments (SVF), number of rivers and streams (RS), number of tree lines (TL), type of topography (TT), percent vegetation (%V), number of buildings (B), number of roads (Ro), type of management (TM), size of herd examined (SH), number of head of cattle in 200 m (H200m) and number of head of other livestock in 500 m (OTL500m). Model Model Variables K Deviance Pseudo-R2 AIC Movement facilitation TT+SVF+LVF+RS+%V+TL 7 55.5 0.033 363.9 Human interference B+R 3 54.7 0.047 355.1 Prey availability TM+H200m+OTL500m+SH 5 55.5 0.032 360.0 Combined TT+ Ro+OTL500m 4 53.0 0.076 363.9

Table 2. Variables included in the two models that explained the highest proportion of deviance of incidence of attacks (human interference model and combined model) in 61 sampling units in northeastern Puebla. The value of the β coefficient, its confidence limits, and its significance are reported. Variables β Coef. Confidence interval Chi-squared Significance Lower limit Upper limit Human interference model Number of roads -0.248 -0.564 0.068 2.371 0.124 Number of buildings -0.026 -0.129 0.076 0.253 0.615 Combined model Type of topography -0.041 -0.181 0.100 0.324 0.569 Number of roads -0.321 -0.942 0.300 1.025 0.311 Other type of livestock <500 m -0.300 -0.637 0.037 3.050 0.081

The information accumulated by multiple studies in- dus does not leave its roost to forage until there is dicates that D. rotundus has a marked lunar phobia, complete darkness (Wimsatt 1969). Flores-Crespo et that is, it tends to reduce its activity during nights or at al. (1972) suggested that the habit of foraging during times at night with high levels of moonlight (Saldaña- the darkest hours of the night is probably because D. Vázquez and Munguía-Rosas 2013). In agreement rotundus perceives light as a factor that increases the with this pattern, it has been observed that D. rotun- risk of predation.

www.ujat.mx/era DOI: 10.19136/era.a6n18.2164 ISSN: 2007-9028 E. ISSN: 2007-901X 6 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

Figure 3. Relationship between the incidence of attacks on cattle and the number of buildings in 61 sampling units in northeastern Puebla. According to Pearson’s correlation coefﬁcient, this relationship was not signiﬁcant (r = -0.133, P = 0.305). .

Figure 4. Relationship between the incidence of attacks on cattle and the number of specimens of other livestock species in 61 sampling units in northeastern Puebla. According to Pearson’s correlation coefﬁcient, this relationship was not signiﬁcant (r = -0.148, P = 0.257).

The model associated with movement facilita- mountain areas of the Sierra Madre Oriental, could tion was constructed from landscape-level variables offer shelter and protection to hematophagous bats that could affect the movement of the vampire bat (Medina et al. 2007). In addition, the high availability in the study area. In the northeastern part of the of forest edges and live fences could be used by D. state of Puebla, the landscape is made up of multiple rotundus as ﬂight routes as reported in insectivorous forest or secondary vegetation fragments surrounded species (Brandt et al. 2007). For D. rotundus, which by a matrix of grasslands for cattle ranching. These emits weak vocalizations with a wide range of fre- fragments, which are often associated with karst quencies, linear landscape elements (forest edges,

DOI: 10.19136/era.a6n18.2164 www.ujat.mx/era ISSN: 2007-9028 E. ISSN: 2007-901X 7 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

live fences and streams) could act as reference points According to one of the models generated in for spatial orientation. However, the movement fa- this work (combined model), the frequency of attacks cilitation model was not significant, which could be on cattle is lower when other types of livestock (pigs, due to the fact that, in many locations, large and goats, horses or sheep) are present in the area. This small vegetation fragments could not be included be- result, although not statistically significant, suggests cause they were outside the established scale (200- that other domestic species may represent alterna- m radius). On the other hand, the null relationship tive sources of food for the vampire bat, as has been between the incidence of attacks and the presence of reported in other regions of the continent (Mialhe rivers and streams may be due to most localities being 2014, Bobrowiec et al. 2015), reducing the pressure away from bodies of water. of attack on cattle. The testimonies of cowboys The model describing prey availability was and ranchers seem to support this hypothesis, since established considering each property’s cattle according to them other livestock species are simi- management practices, the presence of other larly attacked by the vampire bat when they are within livestock species in the area, and the size of the fo- reach. cal herd. Results of this model, although with little The low statistical power observed in this work statistical power, seem to contrast with the findings suggests that D. rotundus attacks on cattle may of Delpietro and Russo (1996), who report that the largely depend on variables that were not considered, vampire bat tends to more frequently attack cattle such as the phase of the lunar cycle, the local abun- that are enclosed or tied up. The present study found dance of the vampire bat, prevailing weather con- a higher incidence of attacks in locations where the ditions (heavy rains or winds) or proximity to roosts type of management is controlled grazing (pastures (Moya et al. 2015). The inclusion of a single scale subject to rotation) or free grazing (large or free pas- of analysis may have been a limiting factor for our tures in the mountains); although the results were study, by concealing the effect of factors operating at not statistically significant, the 10 properties with the a wider landscape scale. However, the consistently highest incidence of attacks (> 15%) had this type of low incidence of attacks at sites with a high presence management. On the other hand, four of the six loca- of anthropogenic elements suggests that cattle vacci- tions where cattle were kept in stables or in the yards nation efforts should be more intense in sites further of houses did not record bites. It is likely that the away from villages, ranches and hamlets. structure of the stables or corrals, which usually have walls and roofs, represents an obstacle to the detec- CONCLUSIONS tion of prey by vampires, and these structures tend to be in places where there is anthropogenic move- Although the models generated were not very ment and lighting. For example, Moya et al. (2015) robust, there was a lower incidence of D. rotundus report that the presence of complete roofs in corrals attacks on cattle at nightly resting sites with greater significantly reduces the incidence of attacks on sta- human activity, particularly those surrounded by mul- bled cattle. On the other hand, although larger groups tiple roads (asphalt or dirt roads) and buildings. The were expected to be the most attacked by vampire presence of other livestock species (other than cattle) bats as they are more easily detected, no relationship in the area surrounding the cows’ resting site was was found between the size of the group and the in- negatively related to the incidence of attacks by vam- cidence of attacks. These results are similar to those pire bats. The study of interactions between wildlife reported by Moya et al. (2015), who found that the and human activity is often complex due to the large proximity of vampire bat roosts is a more important number of variables involved. However, the results of predictor of attacks on goats than the number of po- this work provide information to make decisions that tential prey available. favor coexistence between the vampire bat and cattle production.

www.ujat.mx/era DOI: 10.19136/era.a6n18.2164 ISSN: 2007-9028 E. ISSN: 2007-901X 8 Lanzagorta-Valencia et al. Incidence of bites by hematophagous bats Ecosist. Recur. Agropec. 7(1):1-10,2020

ACKNOWLEDGEMENTS not have been possible without the facilities offered by the owners and managers of the ranches, especially The authors wish to thank the following peo- Refugio López, Alejandro Soto, Guillermo Arámburo, ple and institutions that supported and facilitated Domingo Mendoza, René Jaimes, Alejandro Macip the ﬁeld activities: the INIFAP Las Margaritas Ex- and Manuel Varela. Thanks also go to the people perimental Field and its directors René Calderón who assisted us during the ﬁeld work: Juan Hernán- and José de Jesús Mario Ramírez for logistical dez, Enrique González, Carlos Lanzagorta, Cecilia support; and Dolores Manzano (National Campaign Vargas, Jorge San Emeterio and Gerardo Vega. Fi- for the Prevention and Control of Rabies in Cattle nally, we would like to thank Hilda María Díaz López and Livestock Species, Puebla Headquarters) and and Ricardo Alberto Collado Torres for preparing the Filadefo Calderón (Zacapoaxtla jurisdiction) for facili- study area map. tating the selection of cattle ranches. This work would

LITERATURE CITED

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